Skip to main content
Log in

Temperature-Dependent Toxicity of Artemisinin Toward the Macrophyte Lemna minor and the Algae Pseudokirchneriella subcapitata

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Artemisinin, an antimalarial compound derivated from the cultivated plant Artemisia annua L., is produced in situ through cultivation of A. annua under different climatic conditions. The bioactive compound artemisinin has been observed to spread to the surroundings as well as to leach to surface- and groundwater. To make better risk assessments of A. annua which is cultivated under varying climatic conditions, the temperature-dependent toxicity of artemisinin toward the green algae Pseudokirchneriella subcapitata and the macrophyte Lemna minor was evaluated at temperatures ranging from 10 to 30 °C. To include a possible effect of temperature on the degradation rate of artemisinin, artemisinin concentrations were measured during the experiment and toxicity was related to the time-weighted averages of exposure concentrations. The toxicity of artemisinin toward the macrophyte L. minor and the algae P. subcapitata increased with increasing growth rates, and we conclude that bioavailability plays a minor role in the observed relation between temperature and toxicity of artemisinin. The obtained results are important for possible future risk assessment of A. annua cultivation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Arsenault, P. R., Wobbe, K. K., & Weathers, P. J. (2008). Recent advances in artemisinin production through heterologous expression. Current Medicinal Chemistry, 15, 2886–2896.

    Article  CAS  Google Scholar 

  • Chen, P. K., & Leather, G. R. (1990). Plant-growth regulatory activities of artemisinin and its related compounds. Journal of Chemical Ecology, 16, 1867–1876.

    Article  CAS  Google Scholar 

  • Cobb, A.H., Reade, J.P.H., (2010). Herbicides and Plant Physiology. West Sussex: Blackwell Publishing.

  • Dayan, F. E., Hernandez, A., Allen, S. N., Moraes, R. M., Vroman, J. A., Avery, M. A., & Duke, S. O. (1999). Comparative phytotoxicity of artemisinin and several sesquiterpene analogues. Phytochemistry, 50, 607–614.

    Article  CAS  Google Scholar 

  • Delabays, N., Simonnet, X., & Gaudin, M. (2001). The genetics of artemisinin content in Artemisia annua L. and the breeding of high yielding cultivars. Current Medicinal Chemistry, 8, 1795–1801.

    Article  CAS  Google Scholar 

  • Dhingra, V., Rao, K. V., & Narasu, M. L. (2000). Current status of artemisinin and its derivatives as antimalarial drugs. Life Sciences, 66, 279–300.

    Article  CAS  Google Scholar 

  • Duke, S. O., Vaughn, K. C., Croom, E. M., & El Sohly, H. N. (1987). Artemisinin, a constituent of annual wormwood (Artemisia annua), is a selective phytotoxin. Weed Science, 35, 499–505.

    CAS  Google Scholar 

  • Efferth, T., Romero, M. R., Wolf, D. G., Stamminger, T., Marin, J. J. G., & Marschall, M. (2008). The antiviral activities of artemisinin and artesunate. Clinical Infectious Diseases, 47, 804–811.

    Article  CAS  Google Scholar 

  • Ferreira, J. F. S., Laughlin, J. C., Delabays, N., & Magalhães, P. M. (2005). Cultivation and genetics of Artemisia annua L. for increased production of the antimalarial artemisinin. Plant Genetic Resources, 3, 206–229.

    Article  CAS  Google Scholar 

  • Giddings, J. M., Anderson, T. A., Hall, L. W., Jr., Hosmer, A. J., Kendall, R. J., Richards, R. P., Solomon, K. R., & Williams, W. M. (2005). Tier 3 risk assessment. Atrazine in North American Surface Waters - a probailistic aquatic ecological risk assessment (pp. 85–140). Pensacola: SETAC.

    Google Scholar 

  • Herrmann, S., Jessing, K. K., Joergensen, N. O. G., Cedergreen, N., Kandler, E., & Strobel, B. W. (2013). Distribution and ecological impact of artemisinin derived from Artemisia annua L. in an agricultural ecosystem. Soil Biology & Biochemistry, 57, 164–172.

    Article  CAS  Google Scholar 

  • International Organization for standardization. (1989). Water quality—fresh water algal growth inhibition test with Scenedesmus subspicatus and Selenastrum capricornutum. ISO:8692. Geneva: International Organization for standardization.

  • International Organization for standardization. (2004). Water quality—duckweed growth inhibition. ISO/WD 20079. Geneva: International Organization for Standardization.

  • Jessing, K., Bowers, T., Strobel, B. W., Svensmark, B., & Hansen, H. C. (2009a). Artemisinin determination and degradation in soil using supercritical fluid extraction and HPLC-UV. International Journal of Environmental Analytical Chemistry, 89, 1–10.

    Article  CAS  Google Scholar 

  • Jessing, K. K., Cedergreen, N., Jensen, J., & Hansen, H. C. (2009b). Degradation and ecotoxicity of the biomedical drug artemisinin in soil. Environmental Toxicology and Chemistry, 28, 701–710.

    Article  CAS  Google Scholar 

  • Jessing, K. K., Juhler, R. K., & Strobel, B. W. (2011). Monitoring of artemisinin, dihydroartemisinin, and artemether in environmental matrices using high-performance liquid chromatography-tandem mass spectrometry (LC-MS/MS). Journal of Agricultural and Food Chemistry, 59, 11735–11743.

    Article  CAS  Google Scholar 

  • Jessing, K. K., Cedergreen, N., Mayer, P., Libous-Bailey, L., Strobel, B. W., Rimando, A., & Duke, S. (2013). Loss of artemisinin produced by Artemisia annua L. to the soil environment. Industrial Crops and Products, 43, 132–140.

    Article  CAS  Google Scholar 

  • Jessing, K. K., Duke, S. O., & Cedergreen, N. (2014). Potential ecological roles of artemisinin produced by Artemisia annua L. Journal of Chemical Ecology, 40, 100–117.

    Article  Google Scholar 

  • Jha, P., Ram, M., Khan, M. A., Kiran, U., Mahmooduzzafar, & Abdin, M. Z. (2011). Impact of organic manure and chemical fertilizers on artemisinin content and yield in Artemisia annua L. Industrial Crops and Products, 33, 296–301.

    Article  CAS  Google Scholar 

  • Klayman, D. L. (1985). Qinghaosu (artemisinin)—an antimalarial drug from China. Science, 228, 1049–1055.

    Article  CAS  Google Scholar 

  • Levesque, F., & Seeberger, P. H. (2012). Continuous-flow synthesis of the antimalaria drug artemisinin. Angewandte Chemie-International Edition, 51, 1706–1709.

    Article  CAS  Google Scholar 

  • Lydon, J., Teasdale, J. R., & Chen, P. K. (1997). Allelopathic activity of annual wormwood (Artemisia annua) and the role of artemisinin. Weed Science, 45, 807–811.

    CAS  Google Scholar 

  • Maeng, J., & Khudairi, A. K. (1973). Studies on the flowering mechanism of Lemna. I. Amino acid changes during flower induction. Physiologia Plantarum, 28, 264–270.

    Article  CAS  Google Scholar 

  • Mayer, P., Cuhel, R., & Nyholm, N. (1997). A simple in vitro fluorescence method for biomass measurements in algal growth inhibition tests. Water Research, 31, 2525–2561.

    Article  CAS  Google Scholar 

  • Meshnick, S. R., Yang, Y. Z., Lima, V., Kuypers, F., Kamchonwongpaisan, S., & Yuthavong, Y. (1993). Iron-dependent free-radical generation from the antimalarial agent artemisinin (Qinghaosu). Antimicrobial Agents and Chemotherapy, 37, 1108–1114.

    Article  CAS  Google Scholar 

  • Panamanik, R. C., Chikkaswamy, B. K., Roy, D. G., Panamanik, A., & Kumar, V. (2008). Effects of biochemicals of Artemisia annua in plants. Journal of Pierre Fauchard Academy, 21, 11–18.

    Google Scholar 

  • Schwarzenbach, R. P., Gschwend, P. M., & Imboden, D. M. (2003). Environmental organic chemistry. Hoboken: Wiley.

    Google Scholar 

  • Stiles, L. H., Leather, G. R., & Chen, P. K. (1994). Effects of two sesquiterpene lactones isolated from Artemisia annua on physiology of Lemna minor. Journal of Chemical Ecology, 20, 969–978.

    Article  CAS  Google Scholar 

  • Tasmin, R., Shimasaki, Y., Tsuyama, M., Qiu, X., Khalil, F., Okino, N., Yamada, N., Fukuda, S., Kang, I.-K., & Oshima, Y. (2014). Elevated water temperature reduces the acute toxicity of the widely used herbicide diuron to a green alga, Pseudokirchneriella subcapitata. Environmental Science and Pollution Research, 21, 1064–1070.

    Article  CAS  Google Scholar 

  • van der Heide, T., Roijackers, R. M. M., van Nes, E. H., & Peeters, E. T. H. M. (2006). Simple equation for describing the temperature dependent growth of free-floating macrophytes. Aquatic Botany, 84, 171–175.

    Article  Google Scholar 

  • Weiner, J. A., DeLorenzo, M. E., & Fulton, M. H. (2004). Relationship between uptake capacity and differential toxicity of the herbicide atrazine in selected microalgal species. Aquatic Toxicology, 68, 121–128.

    Article  CAS  Google Scholar 

  • Wetzel, R. G. (1983). Limnology. Orlando: Saunders Collage Publishing.

    Google Scholar 

  • WHO (2010). World malaria report. 1-238. Geneva: World Health Organization.

    Google Scholar 

  • WHO (2011). World malaria report, FACT SHEET. World Health Organization. Global Malaria Programme.

  • Wu, Y. K., & Liu, H. H. (2003). Cleavage of qinghaosu (artemisinin) induced by non-iron transition-metal ions in the presence of excess cysteine. Helvetica Chimica Acta, 86, 3074–3080.

    Article  CAS  Google Scholar 

  • Zhao, S.S. & Zeng, M.Y. (1985). Spektrometische Hochdruck-Flüssigkeits-Chromatographische (HPLC) Untersuchungen zur Analytik von Qinghaosu. Planta Medica 51, 233-237.

Download references

Acknowledgments

We wish to thank the Department of Basic Sciences and Environment, Faculty of Life Science, University of Copenhagen, who supported this work financially.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Karina K. Jessing.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jessing, K.K., Andresen, M. & Cedergreen, N. Temperature-Dependent Toxicity of Artemisinin Toward the Macrophyte Lemna minor and the Algae Pseudokirchneriella subcapitata . Water Air Soil Pollut 225, 2010 (2014). https://doi.org/10.1007/s11270-014-2010-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-014-2010-1

Keywords

Navigation